Visual-Vestibular interaction in motion perception

Self-motion perception relies primarily on the integration of the visual, vestibular, proprioceptive, and somatosensory systems. There is a gap in understanding how a temporal lag between visual and vestibular motion cues affects visual-vestibular weighting during self-motion perception. The beta band is an index of visual-vestibular weighting, in that robust beta event-related synchronization (ERS) is associated with visual weighting bias, and robust beta event-related desynchronization is associated with vestibular weighting bias. The present study examined modulation of event-related spectral power during a heading judgment task in which participants attended to either visual (optic flow) or physical (inertial cues stimulating the vestibular, proprioceptive and somatosensory systems) motion cues from a motion simulator mounted on a MOOG Stewart Platform. The temporal lag between the onset of visual and physical motion cues was manipulated to produce three lag conditions: simultaneous onset, visual before physical motion onset, and physical before visual motion onset. There were two main findings. First, we demonstrated that when the attended motion cue was presented before an ignored cue, the power of beta associated with the attended modality was greater than when visual-vestibular cues were presented simultaneously or when the ignored cue was presented first. This was the case for beta ERS when the visual-motion cue was attended to, and beta event-related desynchronization when the physical-motion cue was attended to. Second, we tested whether the power of feature-binding gamma ERS (demonstrated in audiovisual and visual-tactile integration studies) increased when the visual-vestibular cues were presented simultaneously versus with temporal asynchrony. We did not observe an increase in gamma ERS when cues were presented simultaneously, suggesting that electrophysiological markers of visual-vestibular binding differ from markers of audiovisual and visual-tactile integration. All event-related spectral power reported in this study were generated from dipoles projecting from the left and right motor areas, based on the results of Measure Projection Analysis.

In the real world in which we move around, inertial and visual motion are usually equal; what you see is what you feel. In a simulator, however, this is usually not the case. On the contrary, due to the relatively small motion space of even the largest simulators, the inertial motion cues must be filtered and scaled down considerably. Typically, inertial motion cues are high-pass filtered and scaled down by as much as fifty to seventy percent in a flight simulator. This does not necessarily mean that the motion simulation is unnatural or unconvincing, since certain differences between inertial and visual motion cannot be detected by the human perceptual system. Especially, when the visual scene has rich content with a lot of detail, high-contrast and a wide field-of-view. The maximum allowable difference between visual and inertial motion that goes undetected is defined as the visual-vestibular coherence zone. Knowledge of these coherence zones is very valuable for the development of effective simulator motion cueing. The results of the yaw motion perception experiment described in this paper provide strong indications that the coherence zone between visual and inertial yaw motion is not simply determined by a simple gain or threshold, but is frequency dependent. From a perception modeling point-of-view one can argue that the frequency dependency is related to the inverse dynamics of the semi-circular canals. The experimental findings support this argument, although further research is required to determine a more precise dynamic coherence zone and to test other degrees-of-freedom. Copyright © 2009 by Mark Wentink, TNO.

Partial or total unilateral vestibular loss is the third most common cause of peripheral vestibular dysfunction. Dysfunction of one or both of the vestibular mechanisms can manifest physically as abnormalities of posture, balance, and/or visual acuity. This case report describes physical therapy examination and individualized intervention with vestibular rehabilitation for a patient with unilateral vestibular hypofunction. The patient was an 80-year-old male with electronystamographically confirmed unilateral vestibular loss of 98.3%. He demonstrated altered balance and gaze stability classifying him as having an increased risk for falling. After 5 weeks of individualized vestibular rehabilitation, the patient significantly decreased his fall risk from 11 to 20 of 24 on the Dynamic Gait Index. His gaze stability also improved from a 4 to 1 line disparity with dynamic visual acuity testing. The patient also had a decrease in perceived disability on the Dizziness Handicap Inventory from 30/100 at evaluation to 12/100 at discharge. Individualized vestibular rehabilitation decreased fall risk and improved gaze stability for a patient with significant unilateral vestibular hypofunction.

During a smooth pursuit eye movement of a target stimulus, a briefly flashed stationary background appears to move in the opposite direction as the eye's motion-an effect known as the Filehne illusion. Similar illusions occur in audition, in the vestibular system, and in touch. Recently, we found that the movement of a surface perceived from tactile slip was biased if this surface was sensed with the moving hand. The analogy between these two illusions suggests similar mechanisms of motion processing between the vision and touch. In the present study, we further assessed the interplay between these two sensory channels by investigating a novel paradigm that associated an eye pursuit of a visual target with a tactile motion over the skin of the fingertip. We showed that smooth pursuit eye movements can bias the perceived direction of motion in touch. Similarly to the classical report from the Filehne illusion in vision, a static tactile surface was perceived as moving rightward with a leftward eye pursuit movement, and vice versa. However, this time the direction of surface motion was perceived from touch. The biasing effects of eye pursuit on tactile motion were modulated by the reliability of the tactile and visual stimuli, consistently with a Bayesian model of motion perception. Overall, these results support a modality- and effector-independent process with common representations for motion perception.NEW & NOTEWORTHY The study showed that smooth pursuit eye movement produces a bias in tactile motion perception. This phenomenon is modulated by the reliability of the tactile estimate and by the presence of a visual background, in line with the predictions of the Bayesian framework of motion perception. Overall, these results support the hypothesis of shared representations for motion perception.

One of the first large research projects on human control behavior performed at Delft University of Technology is the work of Hosman and Van der Vaart. In their tracking experiment, Hosman and Van der Vaart investigated the influence of visual and vestibular motion cues on human control behavior in a situation similar to manual control of an aircraft. In these compensatory tracking tasks, subjects were asked to follow or counteract a signal presented on a central (foveal) display. The changes in performance and control behavior were investigated for the addition of peripheral visual and vestibular motion cues. Both disturbance and target following tasks were performed with exactly the same forcing function signal realization. This resulted in a target following and disturbance task which were both thought to be representative for manual control in actual flight, but yielded a significant difference in task difficultybetween both types of task. Because of this discrepancy in task difficulty, it is unsure to what extent the differences between the two types of tracking task observed by Hosman and Van der Vaart actually result from their inherent differences, or are caused by the different levels of task difficulty. This paper describes the results of a recent experiment, highly similar to the tracking experiment of Hosman and Van der Vaart, that was performed in the SIMONA Research Simulator at Delft University of Technology. The goal of this experiment was to measure the effect of different visual and vestibular motion cues on control behavior in compensatory target following and disturbance tasks of equal difficulty, thereby allowing for clear comparison of use of motion cues in both types of tasks. The results of this experiment indicate that the main trends in tracking performance and control behavior reported by Hosman and Van der Vaart for their target following and disturbance tasks can still be seen as representative for both types of classical compensatory tracking task.

Clinical and experimental evidence advocates a structural and functional link between the vestibular and other sensory systems. For instance, visuo-vestibular and vestibular-somatosensory interactions have been widely reported. However, whether visual inputs carrying vestibular information can modulate pain is not yet clear. Recent evidence using natural vestibular stimulation or moving visual stimuli, points at an unspecific effect of distraction. By using immersive virtual reality (VR), we created a new way to prompt the vestibular system through the vision of static visual cues, studying the possible interaction with pain. Twenty-four healthy participants were visually immersed in a virtual room which could appear with five different degrees of rotation in the sagittal axis, either towards the right, left or with no rotation. Participants' heat pain thresholds and subjective reports of perceived body rotation, sense of presence and attention were measured. 'Being' in a tilted room induced the sensation of body rotation in our participants, even though they were always in an upright position. We also found that rotating the visual scenario can modulate the participants' pain thresholds, determining a significant increase when a left tilt is displayed. In addition,a positive correlation between the perceived body midline rotation and pain threshold wasfoundwhen the virtual room was titled 15 degrees toward the left. Importantly, all VR conditions were found to beequally distractive. Vestibular information present in static visual cues can modulate experimentally-induced acute pain according to a side-dependent manner and bypassing supramodal attentional mechanisms. These findings may help refining pain management approaches based on multimodal stimulation. This study explored how the visualization ofstatic environments in immersive virtual reality can lead to pain threshold modulation through the activation of the vestibular system. Immersion into rotated virtualenvironments led to the illusorysensation of body rotation, and this sensation was found to be related witha modulationof pain perception. Possible analgesic effectsdue to distractioncould beruled out.These results expandour current knowledge about how the visual, vestibular and somatosensory (pain) systems interact. These findings may influence future pain treatmentstrategies based on multisensory stimulation.

Sensory information provided by the vestibular system is crucial in cognitive processes such as the ability to recognize objects. The orientation at which objects are most easily recognized--the perceptual upright (PU)--is influenced by body orientation with respect to gravity as detected from the somatosensory and vestibular systems. To date, the influence of these sensory cues on the PU has been measured using a letter recognition task. Here we assessed whether gravitational influences on letter recognition also extend to human face recognition. 13 right-handed observers were positioned in four body orientations (upright, left-side-down, right-side-down, supine) and visually discriminated ambiguous characters ('p'-from-'d'; 'i'-from-'!') and ambiguous faces used in popular visual illusions ('young woman'-from-'old woman'; 'grinning man'-from-'frowning man') in a forced-choice paradigm. The two transition points (e.g., 'p-to-d' and 'd-to-p'; 'young woman-to-old woman' and 'old woman-to-young woman') were fit with a sigmoidal psychometric function and the average of these transitions was taken as the PU for each stimulus category. The results show that both faces and letters are more influenced by body orientation than gravity. However, faces are more optimally recognized when closer in alignment with body orientation than letters--which are more influenced by gravity. Our results indicate that the brain does not utilize a common representation of upright that governs recognition of all object categories. Distinct areas of ventro-temporal cortex that represent faces and letters may weight bodily and gravitational cues differently--possibly to facilitate the specific demands of face and letter recognition.

We investigated the role of visual feedback in human upright posture control. To make the role of vision clear, we compared the visual, vestibular and somatosensory feedback systems in their ability to perceive movement and suppress short- and long-term sway. First, we measured thresholds for the perception of movement Then effects of each feedback system to suppress short- and long-term sway were analyzed through posture control experiments, in which the available sensory input was limited. The visual and somatosensory thresholds were small ( 0.5 degree). The results of the posture control experiments suggested that the visual system contributed to suppression of sway in the frequency range below 0.4 Hz and the system had a minor effect in frequencies above 0.5 Hz. These results support our previous finding that the visual system does not allow a normal subject to maintain an upright posture by itself. The somatosensory system, on the other hand, suppressed body sway around 0.2 and 0.9 Hz. The higher frequency range might enable the system to maintain an upright posture by itself.

This study investigated multisensory interactions in the perception of auditory and visual motion. When auditory and visual apparent motion streams are presented concurrently in opposite directions, participants often fail to discriminate the direction of motion of the auditory stream, whereas perception of the visual stream is unaffected by the direction of auditory motion (Experiment 1). This asymmetry persists even when the perceived quality of apparent motion is equated for the 2 modalities (Experiment 2). Subsequently, it was found that this visual modulation of auditory motion is caused by an illusory reversal in the perceived direction of sounds (Experiment 3). This "dynamic capture" effect occurs over and above ventriloquism among static events (Experiments 4 and 5), and it generalizes to continuous motion displays (Experiment 6). These data are discussed in light of related multisensory phenomena and their support for a "modality appropriateness" interpretation of multisensory integration in motion perception.

A moving visual field can induce the feeling of self-motion or vection. Illusory motion from static repeated asymmetric patterns creates a compelling visual motion stimulus, but it is unclear if such illusory motion can induce a feeling of self-motion or alter self-motion perception. In these experiments, human subjects reported the perceived direction of self-motion for sway translation and yaw rotation at the end of a period of viewing set visual stimuli coordinated with varying inertial stimuli. This tested the hypothesis that illusory visual motion would influence self-motion perception in the horizontal plane. Trials were arranged into 5 blocks based on stimulus type: moving star field with yaw rotation, moving star field with sway translation, illusory motion with yaw, illusory motion with sway, and static arrows with sway. Static arrows were used to evaluate the effect of cognitive suggestion on self-motion perception. Each trial had a control condition; the illusory motion controls were altered versions of the experimental image, which removed the illusory motion effect. For the moving visual stimulus, controls were carried out in a dark room. With the arrow visual stimulus, controls were a gray screen. In blocks containing a visual stimulus there was an 8s viewing interval with the inertial stimulus occurring over the final 1s. This allowed measurement of the visual illusion perception using objective methods. When no visual stimulus was present, only the 1s motion stimulus was presented. Eight women and five men (mean age 37) participated. To assess for a shift in self-motion perception, the effect of each visual stimulus on the self-motion stimulus (cm/s) at which subjects were equally likely to report motion in either direction was measured. Significant effects were seen for moving star fields for both translation (p = 0.001) and rotation (p<0.001), and arrows (p = 0.02). For the visual motion stimuli, inertial motion perception was shifted in the direction consistent with the visual stimulus. Arrows had a small effect on self-motion perception driven by a minority of subjects. There was no significant effect of illusory motion on self-motion perception for either translation or rotation (p>0.1 for both). Thus, although a true moving visual field can induce self-motion, results of this study show that illusory motion does not.

Self-motion perception and vestibulo-ocular reflex during whole body yaw rotation in standing subjects: The role of head position and neck proprioception

In the nineteenth century Pierre–Jean–Marie Flourens (1825) and Ernst Mach described the vestibular system and its peripheral organs while Robert Barany, rewarded by the Nobel prize in 1914, was the first to investigate vestibular disorders with caloric tests making surgical treatments of the vestibular organ possible. Recently, Graf and Klam (2006) have reminded us that this ancient sensory system appeared more than 500 million years ago. Logically its influence would most likely not be restricted to balance reflexes at the brainstem level; it must have also shaped our brain. The vestibular system is the one sensory organ dedicated to gravity perception, which along with light and oxygen served as a motor of evolution. In the 1950s the groups of Otto–Joachim Grusser in Germany, Wilder Penfield in Canada, and later the group of Alain Berthoz in France, demonstrated in elegant experiments on awake monkey (Guldin and Grusser, 1998), epileptic patient (Penfield, 1957), and neurologically-normal human (Lobel et al., 1999) the existence of vestibular projections to the cortex and how they combine with visual and proprioceptive information. An increasing number of researchers, often fervent disciples, have built on these findings to produce a spate of publications that have consolidated the evidence for a sense of verticality and three-dimensional body representations within the vestibular cortical areas. In the 1990s Paul Smith and colleagues examined vestibular processing in the hippocampus and its role in spatial memory. Exploring this topic in the rodent (Smith, 1997), they began to elucidate the secrets and the previously silent functions of the vestibular system. These findings led to increasing clarity about how vestibular degeneration may be related to some aspects of dementia (Previc, 2013), psychiatric diseases (Gurvich et al., 2013), and cognitive impairments in the elderly (Bigelow et al., 2015; Semenov et al., 2015). The research by Marianne Dieterich and Thomas Brandt has examined the bilateral organization of multiple multisensory cortical areas and revealed the vestibular dominance of the non-dominant hemisphere (Dieterich et al., 2003). They addressed the following questions: how is one global percept of motion and orientation in space formed, and does this dominance determine the lateralization of brain function such as handedness (Brandt and Dieterich, 2015)? A vestibular contribution to the most crucial aspects of the human sense of self and self-consciousness has recently been highlighted by neurological and neuroscientific investigations: vestibular signals contribute to the experience that the self is located within the boundaries of the body (Blanke et al., 2004; Lopez et al., 2008) and may even be involved in self-other discrimination and interactions (Lenggenhager and Lopez, 2015). In this Frontiers in Integrative Neuroscience Research Topic initiated by Sidney Simon, twenty-four articles highlight recent discoveries in the field of vestibular cognition, including: (1) Anatomy of the vestibulo-cortical pathways; (2) Spatial navigation and memory; (3) Spatial cognition, bodily and self-motion perception; (4) Vestibular stimulation and rehabilitation; (5) Posture and motor control; (6) Vestibular disorders and compensation; and (7) Development of vestibular function.

The experiments of Goltz (1870), Mach (1873), Breuer (1891), Ewald (1892), Barany (1907) and Steinhausen (1931, 1933) can be considered as a very important first step in the development of the physiology of the vestibular system. They established a theory of the mechanics of the peripheral vestibular sensory mechanisms which is still basically valid today. The various sensory cells in the peripheral vestibular sensory organ serve as receptors for linear and angular accelerations about different axes, thus providing a three dimensionally organized sensory system for orientation in space. Various other sensory systems such as the visual, somatosensory and acoustic apparatus combine with the vestibular organs in assuring a high sensitivity for the adjustment of the body in space. Part of this regulation is achieved by means of interaction in the vestibular nuclei which integrate the activity of the various vestibular receptors as well as the activity of other sensory structures which converge directly or indirectly on the vestibular neurones. As the vertebrates developed from lower to higher forms other sensory systems such as the somatosensory and visual systems became more and more important in the regulation of posture; however, the vestibular nuclei still remain an important integrative structure that deserves the interest of anatomists as well as physiologists.

Introduction: The aims of the present study were to evaluate postural balance performance of the subjects on the time-restricted feeding (TRF) and reveal the effect of TRF on the vestibular system by comparing the results to those of traditional daily dietary (DD) condition. Methods: Sixteen adults (3 males, 13 females; mean age: 25.4 ± 4 years) who had experienced at least 1 month of TRF were included in the study. The Sensory Organization Test (SOT) and Head-Shake SOT (HS-SOT) – which evaluate proprioceptive, visual, and vestibular systems – were performed on TRF and DD conditions via the Computerized Dynamic Posturography system. Results: Significant differences were obtained between TRF and DD situations in SOT-5 (p = 0.008), SOT-6 (p = 0.01), and HS-SOT5 (p = 0.007) conditions in which the vestibular system dominated. Conclusion: We revealed that TRF has an effect on postural balance in the absence of proprioceptive and visual systems. This feeding model is a negative stressor that has a substantial effect on the vestibular system, but this impact is minimal once the proprioceptive and visual systems are intact. To the best of our knowledge, it is the first study to evaluate postural balance utilizing vestibular parameters in TRF.

The current study aimed at investigating the efficiency of visual, vestibular and somatic sensory systems in postural control of deaf athletes and non-athletes. For this purpose, 30 adolescents aged between 15 and 20 with congenital severe deafness were assigned to athlete and non-athlete groups (mean age 18.08+1.17 yr, height 173.04+6.82 cm and weight 59.41+7.47 kg) by purposive sampling method. A Biodex stabilometer was used to measure the postural control of the subjects in four different sensory conditions to find out the shares of visual, vestibular and somatic systems and the efficiency of each sensory system was calculated by Nashner formula. The SPSS version 18, descriptive statistics and independent t test were used to analyze data (α≤0.05). The results revealed that the efficiency of all sensory systems involved in postural control of deaf athletes was significantly better than deaf non-athletes. The most efficient sensory system involved in postural control was the somatic system in both groups and visual and vestibular systems occupied the next places respectively. It seems that better lower extremity strength and musculoskeletal control in athletes may result in their better balance. Furthermore, the negative effect of the lack of vestibular data in staring process can influence the reduced efficiency of visual system in postural control of deaf subjects. The results of this study can be used to design rehabilitation plans for deaf subjects which show that those musculoskeletal training which improves somatic sensory system may have a greater effect on the balance improvement in the deaf so it is suggested that such training should receive more attention in sport and rehabilitation plans of the deaf.